ZOOTAXA ISSN 1175-5326 (print edition)

ISSN 1175-5334 (online edition)

Accepted by W Sterrer 12 Jul 2019 published 15 Aug 2019Licensed under a Creative Commons Attribution License httpcreativecommonsorglicensesby30

591

Zootaxa 4656 (3) 591ndash595httpswwwmapresscomjzt

Copyright copy 2019 Magnolia PressArticle

httpsdoiorg1011646zootaxa4656313httpzoobankorgurnlsidzoobankorgpub9E91575A-A8BB-4274-9280-191212BE774E

First record of the invasive land flatworm Bipalium adventitium (Platyhelminthes Geoplanidae) in Canada

JEAN-LOU JUSTINE1 5 THOMAS THEacuteRY2 DELPHINE GEY3 amp LEIGH WINSOR4

1 Institut Systeacutematique Eacutevolution Biodiversiteacute (ISYEB) Museacuteum National drsquoHistoire Naturelle CNRS Sorbonne Universiteacute EPHE Universiteacute des Antilles 57 rue Cuvier CP 51 75005 Paris France2 Institut de Recherche en Biologie Veacutegeacutetale (IRBV) Centre sur la Biodiversiteacute 4101 rue Sherbrooke Est H1X2B2 Montreacuteal Queacutebec Canada3 Service de Systeacutematique Moleacuteculaire UMS 2700 Museacuteum National drsquoHistoire Naturelle 57 rue Cuvier CP 26 75005 Paris France4 College of Science and Engineering James Cook University Townsville Australia5 Corresponding author E-mail justinemnhnfr

Summary

Specimens of Bipalium adventitium (Platyhelminthes Geoplanidae) were found in Montreacuteal Queacutebec Canada The specimens showed the typical colour pattern of the species and barcoding (Cytochrome Oxidase I) demonstrated near-identity with a sequence of the same species from the USA This is the first record of the species in Canada

Reacutesumeacute Des speacutecimens de Bipalium adventitium (Plathelminthes Geoplanidae) ont eacuteteacute trouveacutes agrave Montreacuteal Queacutebec Canada Les speacutecimens montraient le motif de couleur typique de lrsquoespegravece et le barcode (cytochrome oxydase I) eacutetait quasi-identique agrave une seacutequence de la mecircme espegravece provenant des Eacutetats-Unis Ceci est la premiegravere mention de lrsquoespegravece au Canada

Land flatworms are transported with earth and pot plants between continents and often become invasive (Justine et al 2014 2015 Winsor 1983) Since land flatworms are predators they constitute a potential danger for the local soil fauna of the areas they invade Among these land flatworms (family Geoplanidae) the hammerhead flatworms (subfamily Bipaliinae) are spectacular by their large size up to one meter their distinctive colours and the typical shape of their head which makes them easy to identify (Winsor 1983) Most species have their origin in Asia but have invaded the world The two ldquogiantrdquo species Bipalium kewense Moseley 1878 and Diversibipalium multilinea-tum (Makino amp Shirasawa 1983) which can be as long as 30 cm have been reported in many locations worldwide (Justine et al 2018b Mazza et al 2016 Morffe et al 2016 Winsor 1983) Bipalium adventitium Hyman 1943 which is smaller but still a noticeable species up to about 10 cm in length is known only from the USA (Hyman 1943 Kawakatsu et al 2002) however since bipaliines do not have their biogeographical origin in North America the species is not a part of the native fauna Rather it is an invasive species known only from its invaded land In this paper we record a finding of Bipalium adventitium in Montreacuteal Canada with identification based on both external morphological and molecular characters Specimens were collected by one of us (TT) One specimen 13 May 2018 Mont Royal Montreacuteal Queacutebec Canada N 455074deg W 736091deg under a stone in a land covered with trees (mainly sugar maple Acer saccharum Marsh northern red oak Quercus rubra L and American basswood Tilia americana L) specimen photographed then lost by the post One specimen 27 May 2018 under a stone Montreacuteal N 455069deg W 736111deg deposited in Museacuteum National drsquoHistoire Naturelle Paris France (MNHN) as MNHN JL327 sampled for molecular analysis One specimen 27 May 2018 under a stone Montreacuteal N 455069deg W 736087deg deposited in MNHN as MNHN JL328 sampled for molecular analysis Two specimens 30 September 2018 Montreacuteal N 455069deg W 736111deg under a stone (in the Collection Entomologique Ouellet-Robert University of Montreacuteal Canada (QMOR) and in T Theacutery Collection France) Four specimens 11 May 2019 Montreacuteal including two under a stone N 455069deg W

brought to you by COREView metadata citation and similar papers at coreacuk

provided by ResearchOnline at James Cook University

JUSTINE ET AL592 middot Zootaxa 4656 (3) copy 2019 Magnolia Press

736110deg and N 455074deg W 736083deg (in the Canadian National Collection of Insects Arachnids and Nematodes Ottawa Canada (CNC) and two under a rotten log N 455072deg W 736083deg (in the Collection of the Insectarium of Montreacuteal Canada (IMQC) and in T Theacutery Collection France) Specimens were collected alive and photographed They were then fixed in pure ethanol and a small portion of the specimen was taken for molecular analysis Se-quences were obtained using our routine protocol (Justine et al 2018b) Briefly genomic DNA was extracted using the QIAamp DNA Mini Kit (Qiagen) Fragments of the COI gene were amplified with the primers BarS COIR JB3 and JB45 PCR products were purified and sequenced in both directions on a 3730xl DNA Analyzer 96-capil-lary sequencer (Applied Biosystems) Results of both analyses were concatenated to obtain a COI sequence of 401 bp in length The sequence was edited using CodonCode Aligner software (CodonCode Corporation Dedham MA USA) compared to the GenBank database content using BLAST and deposited in GenBank under accession number MN192402 and MN192403 MEGA7 (Kumar et al 2016) was used to estimate genetic distances A phy-logenetic analysis was performed with our new sequence and from all sequences available for members of the Bi-paliinae the geographical origin of specimens was checked in publications pertaining to sequences (Aacutelvarez-Presas et al 2008 Justine et al 2018b Moon et al 2011) For the ML tree the best model determined by MEGA7 was the Hasegawa-Kishino-Yano model with discrete Gamma distribution (HKY+G) The specimens about 60 mm in length when alive (Fig 1a) are elongate with the expanded headplate typical of bipaliines tapering to a pointed posterior end The dorsal ground colour was yellow-brown (ldquoRaw Siennardquo) with a fine dark brown median dorsal stripe that does not extend onto the head The headplate is fan-shaped without re-curved lappets and greyish around the anterior margin (Fig 1b) The ventral surface is a pale cream colour The eye pattern and the presence of a gonopore were not examined The external morphology of the specimens accords well with the original description of the species (Hyman 1943)

FiGuRe 1 Living specimens from Montreacuteal Queacutebec a Bipalium adventitium whole specimen dorsal aspect Figure 1 b Bipalium adventitium anterior end dorsal aspect Note the fan-shaped headplate with darker anterior margin and the dark me-dian dorsal stripe that terminates before the headplate

The two specimens JL327 and JL328 had identical COI sequences A tree was built from all sequences available for members of the Bipaliinae for Bipalium kewense Bipalium vagum and Diversibipalium multilineatum since the sequences from various localities are identical (Justine et al 2018b) only one sequence was used The Maximum Likelihood tree is shown in Figure 2 The two sequences of Bipalium adventitium from Montreacuteal Canada formed a monophylum with B adventitium from Kingston Pennsylvania USA indeed for the part of the COI sequence included in the matrix the three sequences are identical The tree provides a clear indication that the species found in Montreacuteal and Kingston is the same however the very low value of most branches precludes any attempts as us-ing the tree to understand phylogenetic relationships between species The distance (p-distance) from B adventitium to the other bipaliine species in the analysis ranged from 126 (B kewense) to 182 (Diversibipalium sp ldquobluerdquo from Mayotte) We noted that two sequences had aberrant positions in the tree HM346597 allegedly B adventitium

BIPALIUM ADVENTITIUM IN CANADA Zootaxa 4656 (3) copy 2019 Magnolia Press middot 593

and HM346600 allegedly D multilineatum these sequences formed a clade with no relation with either of the two species mentioned This may indicate that the original specimens were misidentified The morphological characters colour pattern and the similarity of COI sequence clearly indicate that the speci-mens found in Montreacuteal Queacutebec are B adventitium Bipalium adventitium is a predator of earthworms (Ducey amp Noce 1998 Zaborski 2002) The species actively tracks its prey follows trails of earthworm mucus and can capture earthworms in their tunnels (Fiore et al 2004) It can prey on earthworms 55 times larger than itself in mass (Zabor-ski 2002) The species reproduces by sexual reproduction laying egg capsules that take about 23 days to hatch and contain 1-8 offspring (Ducey et al 2005) As it often occurs with other invasive species it has no known predator and experiments with salamanders and snakes have demonstrated that potential native predators do not consume it (Ducey et al 1999) Bipalium adventitium is one of the two species of terrestrial animals with B kewense in which the presence of tetrodotoxin a powerful neurotoxin has been identified (Stokes et al 2014) An analysis of interactions of invasive and native plants and animals identified Bipalium adventitium as one of the many species involved in complex relationships of what the authors named an ldquoextensive invasional meltdown in North Americardquo (Heimpel et al 2010)

FiGuRe 2 Maximum-likelihood tree of bipaliines based on COI sequences Localities are indicated for specimens For se-quence AF178306 the actual locality is Kingston Pennsylvania USA (erroneously indicated as ldquoLeingston USArdquo) in the paper (Marta Aacutelvarez-Presas personal communication 18 April 2019) Red Bipalium adventitium

After its description based on specimens from California (Hyman 1943) the species has been recorded from a number of US states including California Illinois Massachusetts Michigan Ohio New York Pennsylvania Tennessee and West Virginia (Aacutelvarez-Presas et al 2008 Ducey amp Noce 1998 Ducey et al 2005 Fiore et al 2004 Kawakatsu et al 2002 Stokes et al 2014 Zaborski 2002) A search in GBIF ( httpswwwgbiforgspe-cies5892130) yielded about 80 occurrences (April 2019) mostly from citizen science in various states mainly along the Eastern and Western coasts of the USA The finding in Montreacuteal is probably the Northernmost record of B adventitium in North America and our observations over two years show that the species can survive winter in Queacutebec Bipalium adventitium is a potential threat to the soil fauna and the presence of invasive land flatworms in an additional country should be recorded especially with molecular information (Breugelmans et al 2012 Chaisiri et al 2018 Justine et al 2018a Mazza et al 2016 Morffe et al 2016)

JUSTINE ET AL594 middot Zootaxa 4656 (3) copy 2019 Magnolia Press

The COI sequences of bipaliine species differed by more than 10 suggesting that COI barcode can be reliably used for the identification of species of bipaliines Longer sequences such as complete mitogenomes will be useful in the future (Gastineau et al 2019) In our analysis we remarked that two COI sequences did not group with the species corresponding to the names entered in GenBank when the sequences were deposited these are HM346597 allegedly B adventitium and HM346600 allegedly D multilineatum both from South Korea and both from the same paper (Moon et al 2011) These sequences should not be used for future identification of bipaliine species

Acknowledgements

Marta Aacutelvarez-Presas kindly corrected a misspelling in the Table of her 2008 paper about the locality of the speci-mens from the USA The photographs were taken in Colin Favretrsquos laboratory (Universiteacute de Montreacuteal)

References

Aacutelvarez-Presas M Baguntildeagrave J amp Riutort M (2008) Molecular phylogeny of land and freshwater planarians (Tricladida Platy-helminthes) from freshwater to land and back Molecular Phylogenetics and Evolution 47 555ndash568

httpsdoiorg101016jympev200801032Breugelmans K Quintana Cardona J Artois T Jordaens K amp Backeljau T (2012) First report of the exotic blue land

planarian Caenoplana coerulea (Platyhelminthes Geoplanidae) on Menorca (Balearic Islands Spain) Zookeys 199 91ndash105

httpsdoiorg103897zookeys1993215Chaisiri K Dusitsittipon S Panitvong N Ketboonlue T Nuamtanong S Thaenkham U Morand S amp Dekumyoy P

(2018) Distribution of the newly invasive New Guinea flatworm Platydemus manokwari (Platyhelminthes Geoplanidae) in Thailand and its potential role as a paratenic host carrying Angiostrongylus malaysiensis larvae Journal of Helminthol-ogy 1ndash9 [online]

httpsdoiorg101017S0022149X18000834Ducey PK Messere M Lapoint K amp Noce S (1999) Lumbricid prey and potential herpetofaunal predators of the in-

vading terrestrial flatworm Bipalium adventitium (Turbellaria Tricladida Terricola) American Midland Naturalist 141 305ndash314

httpsdoiorg1016740003-0031(1999)141[0305LPAPHP]20CO2Ducey PK amp Noce S (1998) Successful invasion of New York State by the terrestrial flatworm Bipalium adventitium North-

eastern Naturalist 5 199ndash206 httpsdoiorg1023073858619Ducey PK West L-J Shaw G amp De Lisle J (2005) Reproductive ecology and evolution in the invasive terrestrial planarian

Bipalium adventitium across North America Pedobiologia 49 367ndash377 httpsdoiorg101016jpedobi200504002Fiore C Tull JL Zehner S amp Ducey PK (2004) Tracking and predation on earthworms by the invasive terrestrial planarian

Bipalium adventitium (Tricladida Platyhelminthes) Behavioural Processes 67 327ndash334 httpsdoiorg101016S0376-6357(04)00138-XGastineau R Justine J-L Lemieux C Turmel M amp Witkowski A (2019) Complete mitogenome of the giant invasive

hammerhead flatworm Bipalium kewense Mitochondrial DNA Part B 4 1343ndash1344 httpsdoiorg1010802380235920191596768Heimpel GE Frelich LE Landis DA Hopper KR Hoelmer KA Sezen Z Asplen MK amp Wu K (2010) European

buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America Biological Invasions 12 2913ndash2931

httpsdoiorg101007s10530-010-9736-5Hyman LH (1943) Endemic and exotic land planarians in the United States with a discussion of necessary changes of names

in the Rhynchodemidae American Museum Novitates 1ndash21Justine J-L Lemarcis T Gerlach J amp Winsor L (2018a) First report of the land planarian Endeavouria septemlineata (Hy-

man 1939) (Platyhelminthes Tricladida Continenticola Geoplanidae) in French Polynesia Zootaxa 4450 297ndash300 httpsdoiorg1011646zootaxa4450210Justine J-L Winsor L Barriegravere P Fanai C Gey D Han AWK Quay-Velazquez G La Lee BPY-H Lefevre J-M

Meyer J-Y Philippart D Robinson DG Thevenot J amp Tsatsia F (2015) The invasive land planarian Platydemus ma-nokwari (Platyhelminthes Geoplanidae) records from six new localities including the first in the USA PeerJ 3 e1037

httpsdoiorg107717peerj1037Justine J-L Winsor L Gey D Gros P amp Theacutevenot J (2014) The invasive New Guinea flatworm Platydemus manokwari

in France the first record for Europe time for action is now PeerJ 2 e297

BIPALIUM ADVENTITIUM IN CANADA Zootaxa 4656 (3) copy 2019 Magnolia Press middot 595

httpsdoiorg107717peerj297Justine J-L Winsor L Gey D Gros P amp Theacutevenot J (2018b) Giant worms chez moi Hammerhead flatworms (Platyhel-

minthes Geoplanidae Bipalium spp Diversibipalium spp) in metropolitan France and overseas French territories PeerJ 6 e4672

httpsdoiorg107717peerj4672Kawakatsu M Ogren RE Froehlich EM amp Sasaki G-Y (2002) Additions and corrections of the previous land planar-

ian indices of the world (Turbellaria Seriata Tricladida Terricola) Bulletin of the Fuji Womenrsquos College (Series 2) 40 157ndash177

Kumar S Stecher G amp Tamura K (2016) MEGA7 Molecular Evolutionary Genetics Analysis version 70 for bigger datasets Molecular Biology and Evolution 33 1870ndash1874

httpsdoiorg101093molbevmsw054Mazza G Menchetti M Sluys R Solagrave E Riutort M Tricarico E Justine J-L Cavigioli L amp Mori E (2016) First

report of the land planarian Diversibipalium multilineatum (Makino amp Shirasawa 1983) (Platyhelminthes Tricladida Continenticola) in Europe Zootaxa 4067 (5) 577ndash580

httpsdoiorg1011646zootaxa406754Moon D-H Lee YA amp Huh MK (2011) Identification and phylogenetic relationship at Cytochrome Oxidase Subunit I

(COI) gene among Korean terrestrial planarian taxa Journal of Life Science 21 939ndash946 httpsdoiorg105352JLS2011217939Morffe J Garciacutea N Adams BJ amp Hasegawa K (2016) First record of the land planarian Bipalium kewense Moseley 1878

(Tricladida Geoplanidae Bipaliinae) from Cuba BioInvasions Records 5 127ndash132 httpsdoiorg103391bir20165301Stokes AN Ducey PK Neuman-Lee L Hanifin CT French SS Pfrender ME Brodie E D III amp Brodie Jr ED

(2014) Confirmation and distribution of Tetrodotoxin for the first time in terrestrial invertebrates Two terrestrial flatworm species (Bipalium adventitium and Bipalium kewense) PLoS ONE 9 e100718

httpsdoiorg101371journalpone0100718Winsor L (1983) A revision of the Cosmopolitan land planarian Bipalium kewense Moseley 1878 (Turbellaria Tricladida Ter-

ricola) Zoological Journal of the Linnean Society 79 61ndash100 httpsdoiorg101111j1096-36421983tb01161xZaborski ER (2002) Observations on feeding behavior by the terrestrial flatworm Bipalium adventitium (Platyhelminthes

Tricladida Terricola) from Illinois American Midland Naturalist 148 401ndash408 httpsdoiorg1016740003-0031(2002)148[0401OOFBBT]20CO2

BIPALIUM ADVENTITIUM IN CANADA Zootaxa 4656 (3) copy 2019 Magnolia Press middot 593

and HM346600 allegedly D multilineatum these sequences formed a clade with no relation with either of the two species mentioned This may indicate that the original specimens were misidentified The morphological characters colour pattern and the similarity of COI sequence clearly indicate that the speci-mens found in Montreacuteal Queacutebec are B adventitium Bipalium adventitium is a predator of earthworms (Ducey amp Noce 1998 Zaborski 2002) The species actively tracks its prey follows trails of earthworm mucus and can capture earthworms in their tunnels (Fiore et al 2004) It can prey on earthworms 55 times larger than itself in mass (Zabor-ski 2002) The species reproduces by sexual reproduction laying egg capsules that take about 23 days to hatch and contain 1-8 offspring (Ducey et al 2005) As it often occurs with other invasive species it has no known predator and experiments with salamanders and snakes have demonstrated that potential native predators do not consume it (Ducey et al 1999) Bipalium adventitium is one of the two species of terrestrial animals with B kewense in which the presence of tetrodotoxin a powerful neurotoxin has been identified (Stokes et al 2014) An analysis of interactions of invasive and native plants and animals identified Bipalium adventitium as one of the many species involved in complex relationships of what the authors named an ldquoextensive invasional meltdown in North Americardquo (Heimpel et al 2010)

FiGuRe 2 Maximum-likelihood tree of bipaliines based on COI sequences Localities are indicated for specimens For se-quence AF178306 the actual locality is Kingston Pennsylvania USA (erroneously indicated as ldquoLeingston USArdquo) in the paper (Marta Aacutelvarez-Presas personal communication 18 April 2019) Red Bipalium adventitium

After its description based on specimens from California (Hyman 1943) the species has been recorded from a number of US states including California Illinois Massachusetts Michigan Ohio New York Pennsylvania Tennessee and West Virginia (Aacutelvarez-Presas et al 2008 Ducey amp Noce 1998 Ducey et al 2005 Fiore et al 2004 Kawakatsu et al 2002 Stokes et al 2014 Zaborski 2002) A search in GBIF ( httpswwwgbiforgspe-cies5892130) yielded about 80 occurrences (April 2019) mostly from citizen science in various states mainly along the Eastern and Western coasts of the USA The finding in Montreacuteal is probably the Northernmost record of B adventitium in North America and our observations over two years show that the species can survive winter in Queacutebec Bipalium adventitium is a potential threat to the soil fauna and the presence of invasive land flatworms in an additional country should be recorded especially with molecular information (Breugelmans et al 2012 Chaisiri et al 2018 Justine et al 2018a Mazza et al 2016 Morffe et al 2016)

JUSTINE ET AL594 middot Zootaxa 4656 (3) copy 2019 Magnolia Press

The COI sequences of bipaliine species differed by more than 10 suggesting that COI barcode can be reliably used for the identification of species of bipaliines Longer sequences such as complete mitogenomes will be useful in the future (Gastineau et al 2019) In our analysis we remarked that two COI sequences did not group with the species corresponding to the names entered in GenBank when the sequences were deposited these are HM346597 allegedly B adventitium and HM346600 allegedly D multilineatum both from South Korea and both from the same paper (Moon et al 2011) These sequences should not be used for future identification of bipaliine species

Acknowledgements

Marta Aacutelvarez-Presas kindly corrected a misspelling in the Table of her 2008 paper about the locality of the speci-mens from the USA The photographs were taken in Colin Favretrsquos laboratory (Universiteacute de Montreacuteal)

References

Aacutelvarez-Presas M Baguntildeagrave J amp Riutort M (2008) Molecular phylogeny of land and freshwater planarians (Tricladida Platy-helminthes) from freshwater to land and back Molecular Phylogenetics and Evolution 47 555ndash568

httpsdoiorg101016jympev200801032Breugelmans K Quintana Cardona J Artois T Jordaens K amp Backeljau T (2012) First report of the exotic blue land

planarian Caenoplana coerulea (Platyhelminthes Geoplanidae) on Menorca (Balearic Islands Spain) Zookeys 199 91ndash105

httpsdoiorg103897zookeys1993215Chaisiri K Dusitsittipon S Panitvong N Ketboonlue T Nuamtanong S Thaenkham U Morand S amp Dekumyoy P

(2018) Distribution of the newly invasive New Guinea flatworm Platydemus manokwari (Platyhelminthes Geoplanidae) in Thailand and its potential role as a paratenic host carrying Angiostrongylus malaysiensis larvae Journal of Helminthol-ogy 1ndash9 [online]

httpsdoiorg101017S0022149X18000834Ducey PK Messere M Lapoint K amp Noce S (1999) Lumbricid prey and potential herpetofaunal predators of the in-

vading terrestrial flatworm Bipalium adventitium (Turbellaria Tricladida Terricola) American Midland Naturalist 141 305ndash314

httpsdoiorg1016740003-0031(1999)141[0305LPAPHP]20CO2Ducey PK amp Noce S (1998) Successful invasion of New York State by the terrestrial flatworm Bipalium adventitium North-

eastern Naturalist 5 199ndash206 httpsdoiorg1023073858619Ducey PK West L-J Shaw G amp De Lisle J (2005) Reproductive ecology and evolution in the invasive terrestrial planarian

Bipalium adventitium across North America Pedobiologia 49 367ndash377 httpsdoiorg101016jpedobi200504002Fiore C Tull JL Zehner S amp Ducey PK (2004) Tracking and predation on earthworms by the invasive terrestrial planarian

Bipalium adventitium (Tricladida Platyhelminthes) Behavioural Processes 67 327ndash334 httpsdoiorg101016S0376-6357(04)00138-XGastineau R Justine J-L Lemieux C Turmel M amp Witkowski A (2019) Complete mitogenome of the giant invasive

hammerhead flatworm Bipalium kewense Mitochondrial DNA Part B 4 1343ndash1344 httpsdoiorg1010802380235920191596768Heimpel GE Frelich LE Landis DA Hopper KR Hoelmer KA Sezen Z Asplen MK amp Wu K (2010) European

buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America Biological Invasions 12 2913ndash2931

httpsdoiorg101007s10530-010-9736-5Hyman LH (1943) Endemic and exotic land planarians in the United States with a discussion of necessary changes of names

in the Rhynchodemidae American Museum Novitates 1ndash21Justine J-L Lemarcis T Gerlach J amp Winsor L (2018a) First report of the land planarian Endeavouria septemlineata (Hy-

man 1939) (Platyhelminthes Tricladida Continenticola Geoplanidae) in French Polynesia Zootaxa 4450 297ndash300 httpsdoiorg1011646zootaxa4450210Justine J-L Winsor L Barriegravere P Fanai C Gey D Han AWK Quay-Velazquez G La Lee BPY-H Lefevre J-M

Meyer J-Y Philippart D Robinson DG Thevenot J amp Tsatsia F (2015) The invasive land planarian Platydemus ma-nokwari (Platyhelminthes Geoplanidae) records from six new localities including the first in the USA PeerJ 3 e1037

httpsdoiorg107717peerj1037Justine J-L Winsor L Gey D Gros P amp Theacutevenot J (2014) The invasive New Guinea flatworm Platydemus manokwari

in France the first record for Europe time for action is now PeerJ 2 e297

BIPALIUM ADVENTITIUM IN CANADA Zootaxa 4656 (3) copy 2019 Magnolia Press middot 595

httpsdoiorg107717peerj297Justine J-L Winsor L Gey D Gros P amp Theacutevenot J (2018b) Giant worms chez moi Hammerhead flatworms (Platyhel-

minthes Geoplanidae Bipalium spp Diversibipalium spp) in metropolitan France and overseas French territories PeerJ 6 e4672

httpsdoiorg107717peerj4672Kawakatsu M Ogren RE Froehlich EM amp Sasaki G-Y (2002) Additions and corrections of the previous land planar-

ian indices of the world (Turbellaria Seriata Tricladida Terricola) Bulletin of the Fuji Womenrsquos College (Series 2) 40 157ndash177

Kumar S Stecher G amp Tamura K (2016) MEGA7 Molecular Evolutionary Genetics Analysis version 70 for bigger datasets Molecular Biology and Evolution 33 1870ndash1874

httpsdoiorg101093molbevmsw054Mazza G Menchetti M Sluys R Solagrave E Riutort M Tricarico E Justine J-L Cavigioli L amp Mori E (2016) First

report of the land planarian Diversibipalium multilineatum (Makino amp Shirasawa 1983) (Platyhelminthes Tricladida Continenticola) in Europe Zootaxa 4067 (5) 577ndash580

httpsdoiorg1011646zootaxa406754Moon D-H Lee YA amp Huh MK (2011) Identification and phylogenetic relationship at Cytochrome Oxidase Subunit I

(COI) gene among Korean terrestrial planarian taxa Journal of Life Science 21 939ndash946 httpsdoiorg105352JLS2011217939Morffe J Garciacutea N Adams BJ amp Hasegawa K (2016) First record of the land planarian Bipalium kewense Moseley 1878

(Tricladida Geoplanidae Bipaliinae) from Cuba BioInvasions Records 5 127ndash132 httpsdoiorg103391bir20165301Stokes AN Ducey PK Neuman-Lee L Hanifin CT French SS Pfrender ME Brodie E D III amp Brodie Jr ED

(2014) Confirmation and distribution of Tetrodotoxin for the first time in terrestrial invertebrates Two terrestrial flatworm species (Bipalium adventitium and Bipalium kewense) PLoS ONE 9 e100718

httpsdoiorg101371journalpone0100718Winsor L (1983) A revision of the Cosmopolitan land planarian Bipalium kewense Moseley 1878 (Turbellaria Tricladida Ter-

ricola) Zoological Journal of the Linnean Society 79 61ndash100 httpsdoiorg101111j1096-36421983tb01161xZaborski ER (2002) Observations on feeding behavior by the terrestrial flatworm Bipalium adventitium (Platyhelminthes

Tricladida Terricola) from Illinois American Midland Naturalist 148 401ndash408 httpsdoiorg1016740003-0031(2002)148[0401OOFBBT]20CO2

JUSTINE ET AL594 middot Zootaxa 4656 (3) copy 2019 Magnolia Press

The COI sequences of bipaliine species differed by more than 10 suggesting that COI barcode can be reliably used for the identification of species of bipaliines Longer sequences such as complete mitogenomes will be useful in the future (Gastineau et al 2019) In our analysis we remarked that two COI sequences did not group with the species corresponding to the names entered in GenBank when the sequences were deposited these are HM346597 allegedly B adventitium and HM346600 allegedly D multilineatum both from South Korea and both from the same paper (Moon et al 2011) These sequences should not be used for future identification of bipaliine species

Acknowledgements

Marta Aacutelvarez-Presas kindly corrected a misspelling in the Table of her 2008 paper about the locality of the speci-mens from the USA The photographs were taken in Colin Favretrsquos laboratory (Universiteacute de Montreacuteal)

References

Aacutelvarez-Presas M Baguntildeagrave J amp Riutort M (2008) Molecular phylogeny of land and freshwater planarians (Tricladida Platy-helminthes) from freshwater to land and back Molecular Phylogenetics and Evolution 47 555ndash568

httpsdoiorg101016jympev200801032Breugelmans K Quintana Cardona J Artois T Jordaens K amp Backeljau T (2012) First report of the exotic blue land

planarian Caenoplana coerulea (Platyhelminthes Geoplanidae) on Menorca (Balearic Islands Spain) Zookeys 199 91ndash105

httpsdoiorg103897zookeys1993215Chaisiri K Dusitsittipon S Panitvong N Ketboonlue T Nuamtanong S Thaenkham U Morand S amp Dekumyoy P

(2018) Distribution of the newly invasive New Guinea flatworm Platydemus manokwari (Platyhelminthes Geoplanidae) in Thailand and its potential role as a paratenic host carrying Angiostrongylus malaysiensis larvae Journal of Helminthol-ogy 1ndash9 [online]

httpsdoiorg101017S0022149X18000834Ducey PK Messere M Lapoint K amp Noce S (1999) Lumbricid prey and potential herpetofaunal predators of the in-

vading terrestrial flatworm Bipalium adventitium (Turbellaria Tricladida Terricola) American Midland Naturalist 141 305ndash314

httpsdoiorg1016740003-0031(1999)141[0305LPAPHP]20CO2Ducey PK amp Noce S (1998) Successful invasion of New York State by the terrestrial flatworm Bipalium adventitium North-

eastern Naturalist 5 199ndash206 httpsdoiorg1023073858619Ducey PK West L-J Shaw G amp De Lisle J (2005) Reproductive ecology and evolution in the invasive terrestrial planarian

Bipalium adventitium across North America Pedobiologia 49 367ndash377 httpsdoiorg101016jpedobi200504002Fiore C Tull JL Zehner S amp Ducey PK (2004) Tracking and predation on earthworms by the invasive terrestrial planarian

Bipalium adventitium (Tricladida Platyhelminthes) Behavioural Processes 67 327ndash334 httpsdoiorg101016S0376-6357(04)00138-XGastineau R Justine J-L Lemieux C Turmel M amp Witkowski A (2019) Complete mitogenome of the giant invasive

hammerhead flatworm Bipalium kewense Mitochondrial DNA Part B 4 1343ndash1344 httpsdoiorg1010802380235920191596768Heimpel GE Frelich LE Landis DA Hopper KR Hoelmer KA Sezen Z Asplen MK amp Wu K (2010) European

buckthorn and Asian soybean aphid as components of an extensive invasional meltdown in North America Biological Invasions 12 2913ndash2931

httpsdoiorg101007s10530-010-9736-5Hyman LH (1943) Endemic and exotic land planarians in the United States with a discussion of necessary changes of names

in the Rhynchodemidae American Museum Novitates 1ndash21Justine J-L Lemarcis T Gerlach J amp Winsor L (2018a) First report of the land planarian Endeavouria septemlineata (Hy-

man 1939) (Platyhelminthes Tricladida Continenticola Geoplanidae) in French Polynesia Zootaxa 4450 297ndash300 httpsdoiorg1011646zootaxa4450210Justine J-L Winsor L Barriegravere P Fanai C Gey D Han AWK Quay-Velazquez G La Lee BPY-H Lefevre J-M

Meyer J-Y Philippart D Robinson DG Thevenot J amp Tsatsia F (2015) The invasive land planarian Platydemus ma-nokwari (Platyhelminthes Geoplanidae) records from six new localities including the first in the USA PeerJ 3 e1037

httpsdoiorg107717peerj1037Justine J-L Winsor L Gey D Gros P amp Theacutevenot J (2014) The invasive New Guinea flatworm Platydemus manokwari

in France the first record for Europe time for action is now PeerJ 2 e297

BIPALIUM ADVENTITIUM IN CANADA Zootaxa 4656 (3) copy 2019 Magnolia Press middot 595

httpsdoiorg107717peerj297Justine J-L Winsor L Gey D Gros P amp Theacutevenot J (2018b) Giant worms chez moi Hammerhead flatworms (Platyhel-

minthes Geoplanidae Bipalium spp Diversibipalium spp) in metropolitan France and overseas French territories PeerJ 6 e4672

httpsdoiorg107717peerj4672Kawakatsu M Ogren RE Froehlich EM amp Sasaki G-Y (2002) Additions and corrections of the previous land planar-

ian indices of the world (Turbellaria Seriata Tricladida Terricola) Bulletin of the Fuji Womenrsquos College (Series 2) 40 157ndash177

Kumar S Stecher G amp Tamura K (2016) MEGA7 Molecular Evolutionary Genetics Analysis version 70 for bigger datasets Molecular Biology and Evolution 33 1870ndash1874

httpsdoiorg101093molbevmsw054Mazza G Menchetti M Sluys R Solagrave E Riutort M Tricarico E Justine J-L Cavigioli L amp Mori E (2016) First

report of the land planarian Diversibipalium multilineatum (Makino amp Shirasawa 1983) (Platyhelminthes Tricladida Continenticola) in Europe Zootaxa 4067 (5) 577ndash580

httpsdoiorg1011646zootaxa406754Moon D-H Lee YA amp Huh MK (2011) Identification and phylogenetic relationship at Cytochrome Oxidase Subunit I

(COI) gene among Korean terrestrial planarian taxa Journal of Life Science 21 939ndash946 httpsdoiorg105352JLS2011217939Morffe J Garciacutea N Adams BJ amp Hasegawa K (2016) First record of the land planarian Bipalium kewense Moseley 1878

(Tricladida Geoplanidae Bipaliinae) from Cuba BioInvasions Records 5 127ndash132 httpsdoiorg103391bir20165301Stokes AN Ducey PK Neuman-Lee L Hanifin CT French SS Pfrender ME Brodie E D III amp Brodie Jr ED

(2014) Confirmation and distribution of Tetrodotoxin for the first time in terrestrial invertebrates Two terrestrial flatworm species (Bipalium adventitium and Bipalium kewense) PLoS ONE 9 e100718

httpsdoiorg101371journalpone0100718Winsor L (1983) A revision of the Cosmopolitan land planarian Bipalium kewense Moseley 1878 (Turbellaria Tricladida Ter-

ricola) Zoological Journal of the Linnean Society 79 61ndash100 httpsdoiorg101111j1096-36421983tb01161xZaborski ER (2002) Observations on feeding behavior by the terrestrial flatworm Bipalium adventitium (Platyhelminthes

Tricladida Terricola) from Illinois American Midland Naturalist 148 401ndash408 httpsdoiorg1016740003-0031(2002)148[0401OOFBBT]20CO2

BIPALIUM ADVENTITIUM IN CANADA Zootaxa 4656 (3) copy 2019 Magnolia Press middot 595

httpsdoiorg107717peerj297Justine J-L Winsor L Gey D Gros P amp Theacutevenot J (2018b) Giant worms chez moi Hammerhead flatworms (Platyhel-

minthes Geoplanidae Bipalium spp Diversibipalium spp) in metropolitan France and overseas French territories PeerJ 6 e4672

httpsdoiorg107717peerj4672Kawakatsu M Ogren RE Froehlich EM amp Sasaki G-Y (2002) Additions and corrections of the previous land planar-

ian indices of the world (Turbellaria Seriata Tricladida Terricola) Bulletin of the Fuji Womenrsquos College (Series 2) 40 157ndash177

Kumar S Stecher G amp Tamura K (2016) MEGA7 Molecular Evolutionary Genetics Analysis version 70 for bigger datasets Molecular Biology and Evolution 33 1870ndash1874

httpsdoiorg101093molbevmsw054Mazza G Menchetti M Sluys R Solagrave E Riutort M Tricarico E Justine J-L Cavigioli L amp Mori E (2016) First

report of the land planarian Diversibipalium multilineatum (Makino amp Shirasawa 1983) (Platyhelminthes Tricladida Continenticola) in Europe Zootaxa 4067 (5) 577ndash580

httpsdoiorg1011646zootaxa406754Moon D-H Lee YA amp Huh MK (2011) Identification and phylogenetic relationship at Cytochrome Oxidase Subunit I

(COI) gene among Korean terrestrial planarian taxa Journal of Life Science 21 939ndash946 httpsdoiorg105352JLS2011217939Morffe J Garciacutea N Adams BJ amp Hasegawa K (2016) First record of the land planarian Bipalium kewense Moseley 1878

(Tricladida Geoplanidae Bipaliinae) from Cuba BioInvasions Records 5 127ndash132 httpsdoiorg103391bir20165301Stokes AN Ducey PK Neuman-Lee L Hanifin CT French SS Pfrender ME Brodie E D III amp Brodie Jr ED

(2014) Confirmation and distribution of Tetrodotoxin for the first time in terrestrial invertebrates Two terrestrial flatworm species (Bipalium adventitium and Bipalium kewense) PLoS ONE 9 e100718

httpsdoiorg101371journalpone0100718Winsor L (1983) A revision of the Cosmopolitan land planarian Bipalium kewense Moseley 1878 (Turbellaria Tricladida Ter-

ricola) Zoological Journal of the Linnean Society 79 61ndash100 httpsdoiorg101111j1096-36421983tb01161xZaborski ER (2002) Observations on feeding behavior by the terrestrial flatworm Bipalium adventitium (Platyhelminthes

Tricladida Terricola) from Illinois American Midland Naturalist 148 401ndash408 httpsdoiorg1016740003-0031(2002)148[0401OOFBBT]20CO2